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Chapter 8

Sorghum and its Weedy Hybrids

Gebisa Ejeta and Cécile Grenier

Dept. of Agronomy, Lilly Hall of Life Sciences, 915 W. State Street, Purdue University, West Lafayette, IN 47907, U.S.A. [email protected]

1. INTRODUCTION

Genetic exchange between wild and cultivated sorghums occurs in nature. The appearance of weedy traits such as shattering and rhizomatousness (development of that propagate from rhizomes) in -wild hybrids of sorghum has often been used as evidence for such exchanges. The impact of unusual traits resulting from these introgressions in the nature of the resultant hybrids including the appearance of feral forms has not been widely studied and documented. Sorghum is one of the five most important in the world, and mainly cultivated in the developing world including , the ancestral home of the crop. In many of these areas, volunteer, wild, and weedy forms exist both together with the crop and in nearby ruderal areas. Intermediary forms such as shattercanes are ubiquitous and exist in a continuum of forms ranging from those that closely resemble the wild to those very nearly indistinguishable from the cultivated members of the same . While there is no clear evidence for the existence of feral types emerging as a result of mutational de- (endo-ferality), the existence of intermediary forms in most sorghum growing areas offers an empirical evidence for noxious weedy forms arising from continued introgression (exo-ferality) among different sorghum types. For instance, the most widely recognized noxious weed in the sorghum taxa, Sorghum halepense (johnsongrass), is a natural hybrid between the cultivated and wild rhizomatous species S. propinquum. With the advent of the transgenic era, genetic transformation of sorghums has been approached with some apprehension among sorghum research scientists. If developed, the deployment of transgenic sorghums is likely to be met with some trepidation due primarily to the concern that feral transgenic hybrid forms that are more fit and difficult to eradicate may arise as a result of natural and accidental cross . Research is needed to assess the extent of spontaneous gene flow among the cultivated-wild-weed complex of the sorghum taxa and, should there appear some danger, to devise means for its mitigation. In this chapter we describe the sorghum taxa, the nature of the profile of the crop-wild-weed complex in sorghum, and the existence of intermediary forms of varying ferality, relative to the ease of genetic exchange among the species in the taxa. The influence of the agro-ecosystem in modifying the natural habitat, in catalyzing effective genetic exchange, and in disseminating the resultant hybrid forms is also discussed using anecdotal evidence from three major sorghum growing environments around the world.

2. THE SORGHUM TAXA

The genus sorghum belongs to the (Gramineae) family. Along with (Zea mays), (Saccharum spp.), and all the (Pennisetum, Eleusine, Eragrostis, Setaria, etc.),

1 it falls into the tribe . The genus sorghum is divided into five sub-genera: Eu- Sorghum, Parasorghum, Heterosorghum, Chaetosorghum and Stiposorghum (Fig.1). Three species are recognized in the sub-genera Sorghum (Eu-Sorghum) including the two rhizomatous weedy taxa, Sorghum halepense (L.) Pers. and S. propinquum (Kunth.) Hitchc., as well as cultivated sorghum S. bicolor (L.) Moench, which also has weedy forms. According to Harlan and de Wet (21), S. bicolor and S. propinquum are found in the primary gene pool (GP-1) of sorghum, which contains biological species of both the cultivated and spontaneous (wild and/or weedy) races. The species in this primary gene pool intercross readily and produce fertile hybrids. S. halepense is found in the secondary gene pool (GP-2) which includes all species that can be crossed with GP-1 with at least some fertility in the hybrids. This suggests that gene transfer between these two gene pools is possible, though it may be difficult in some situations. The other sections of the sorghum taxa are encompassed in the tertiary gene pool (GP-3) where hybrids with GP-1 are anomalous, lethal or nearly completely sterile, and gene transfer is not readily possible or requires radical techniques (Fig. 2). Sorghum bicolor is indigenous to Africa. It includes the weedy type sorghums classified under S. bicolor drummondii, the wild progenitor S. b. arundinaceum, and the cultivated crop, S. b. bicolor (Fig. 1). Members of the S. bicolor subspecies are diploid (2n=20). Cultivated sorghum in much of the world is sympatric with other sexually compatible, cultivated and feral relatives (2). is a strongly-rhizomatous perennial indigenous to , and freely introgresses with its congener, S. bicolor. Sorghum halepense, also a perennial, is a tetraploid (2n=40) species. Both its rhizomatous nature and its geographical distribution suggest that S. halepense is an interspecific hybrid derived as a descendant of S. bicolor and S. propinquum (34, 35).

2.1 CULTIVATED SORGHUMS

The pattern of distribution and history of domestication of sorghum has been carefully delineated in a series of insightful observations by early botanists (22, 31, 40, 42). Cultivated sorghum arose from the wild Sorghum bicolor subsp. arundianaceum (28). There is no evidence suggesting that presently cultivated sorghums have evolved from the rhizomatous diploid or tetraploid wild species (10). Domestication of the sorghum crop is presumed to have started in the north-east quadrant of Africa (22) some 5,000 years ago perhaps in the expanse of arable land area recognized in contemporary geography as Ethiopia and Sudan. The great genetic variability of the crop in this geographical area, the wide range of ecological habitats there, and the long history of human selection efforts in the region have given sufficient credence to the theory of the origin and early domestication of sorghum in eastern Africa. Several routes have been recognized for the later movement of sorghum into other parts of Africa and beyond (Fig. 3). Early movement between 2,000 and 4,000 years ago has taken the crop to west, central, and southern Africa leading to further domestication and appearance of distinct forms (races) in each of these regions. Harlan and de Wet (22) recognize five major races and ten intermediate "hybrid" forms having arisen from these early movement of S. bicolor. Of the sorghum races, bicolor was domesticated first (11). Bicolors are grown across the range of sorghum cultivation in Africa. Race caudatum is an old race of grain sorghum, still widely grown in present Chad, Sudan, northeastern and Uganda. The race guinea, while occasionally cultivated in several places around the world is uniquely predominant in the west African savannah. The durra race is preponderant in the Ethiopian and Yemen highlands. Durras are widely grown along the

2 fringes of the southern Sahara, across arid west-Africa, whereas race kafir is distinctly eastern and southern African from Tanzania southward. Beyond Africa, early domestication of sorghum took place also in the Indian sub-continent about 3,000 years ago having moved there very early both over the as well as over the Arabian peninsula. The small-panicled, dryland durras commonly found in India today are distinctly different in form, adaptation, stress tolerance, as well as overall productivity from those found in the east African highlands. Distinctly later than in these early movements, sorghum was also moved from India to over the Himalayas as evidenced by appearance of new races of sorghum. Chinese kaoliangs uniquely make up the only sorghums in the world that have evolved in the temperate parts of the world. As a result, they have become an invaluable source of early season cold tolerance in sorghum. Even much more recently, sorghum was moved from Africa in the last three centuries, via the slave trade, to the Americas. Evidence for distinct evolutionary changes is limited in the Americas, yet sorghum received its greatest transformation as a crop through modern selection efforts and mechanized cultivation. Today, cultivated sorghum is one of the most economically important crops of the world with an annual production of ~60 million metric tons (15). It is used in a wide array of forms and for a range of purposes, constituting an essential portion of the diet of people living in the semi-arid tropics. The United States, India, and Nigeria together produce nearly half of the grain sorghum harvested annually around the world. Among African countries, Nigeria (8.1 million tons), Sudan (4.4 million tons) and Ethiopia (1.6 million tons) are the largest producers of grain sorghum. Sorghum is most widely grown in the semi arid tropics. Of the total land area of 95.2 million ha annually committed to production in Africa, over 24.3 million ha of the arable land is cultivated with sorghum (15). In some nations, such as the Sudan, sorghum is very important and widely cultivated providing the nutritional backbone of the population with grain harvested on more than 65% of the total area allocated to (18). Sorghum is well adapted to a wide range of environmental conditions. It is generically drought and flood tolerant, and often does well in both heavy and light sandy soils over a pH range of 5.5 to 8.5, and can also withstand high salinity levels. Sorghum has a number of morphological and physiological characteristics that contribute to its adaptation to contrasting moisture, temperature, and as well as varying soil fertility and ecological conditions. In spite of its broad adaptation and being fit to a range of harsh environments, sorghum production can be constrained by biotic and abiotic stresses. Insects, diseases, parasitic weeds, as well as severe deficits and erratic distribution of rainfall in drier areas often devastate sorghum crops. However, the great wealth of genetic diversity in the species has allowed both natural and artificial selection efforts to result in continual progress in deriving hardier variants of the species. Several breeding programs have successfully identified sources of agronomically-valuable genes within the sorghum germplasm and effectively introduced them into improved varieties adapted to cultivation under various environmental conditions. The use of molecular marker assisted selection offers promise for faster and even more efficient crop breeding. Though no sorghum cultivar has yet been developed and released through marker assisted selection, techniques have been developed and molecular markers identified promising a more deliberate and rapid incorporation of traits into preferred germplasm backgrounds. Furthermore, new tools promise an even faster rate of progress and a more precise mode of incorporating new genes in existing cultivars in a crop improvement program. Genetic transformation of sorghum has been pursued, in recent years, to genetically engineer special purpose sorghums. Although stable transformations were obtained through biolistic bombardment (5, 24) and Agrobacterium mediated transformation (44) further improvements are

3 needed to achieve more reliable transformation protocols before transgenic sorghums can be more readily exploited. With efficient transformation systems in sorghum and other cereal species, valuable genes selected from an organism in the same or different species, family, tribe or even from an organism belonging to a different kingdom could more precisely and readily be transferred into a crop, a feat so unimaginable in natural selection or traditional selection efforts of the past.

2.2 WILD AND WEEDY SORGHUMS

Domestication of sorghum began with wild members of Sorghum bicolor subsp. arundinaceum. Ecological and geographical isolation probably gave rise to the following four races of wild sorghums from S. b. arundinaceum (21). • Race aethiopicum formed part of the grass vegetation across the drier parts of the west African savannah, extending from western Ethiopia to Mauritania. This race can be locally very abundant appearing in large tracts of land and occasionally invades cultivated fields. • Race arundinaceum is a forest grass widely distributed in moist tropical forests of the Guinea coast and the Congo. It appears as a common grass along stream banks and forest paths, and occasionally establishes in cultivated fields. • Race verticilliflorum is a common grass across most of the African savannah, between Sudan and Nigeria, found in weedy patches along roadsides, and often found established in cultivated fields. It is the most widely distributed wild sorghum, having been introduced to tropical , parts of India and the New World (8). Along with race aethiopicum, it is found most everywhere sorghum is grown in Sudan. • Race virgatum is a desert grass distributed along irrigation ditches and streambanks in central Sudan and extends along the length of the Nile northwards to Cairo. Weedy sorghums exist parallel to the wild sorghums, as either the perennial rhizomatous forms derived from Sorghum propinquum or the annual grassy weeds that resulted from hybridization between cultivated and wild sorghums within the Sorghum bicolor species. Sorghum propinquum is a strongly-rhizomatous, perennial species indigenous to Asia. Ecologically, S. propinquum thrives as a forest grass well adapted to moist habitats such as river banks. The pattern of evolutionary changes for weedy sorghum types suggests an ancestral diploid species common to the wild grass S. bicolor arundinaceum and the diploid perennial S. propinquum (10). It is suspected that one prototype spread into southeast Asia where the humid climates and high rainfall favored the development of rhizomes, while a second form spread into north-east Africa in a habitat of open country with long dry seasons, where the annual growth habit of the plant was favored (Fig. 3). The primary geographical area of occurrence for S. propinquum is the Indian subcontinent, and includes the area from Burma eastward to the islands of southeastern Asia. This species readily crosses with the introduced grain sorghums in the Philippines and derivatives of such crosses are recognized as noxious weeds. S. halepense is a perennial, tetraploid sorghum native of southern Eurasia, east of India. It occupies a continuous area from southern and eastern India to the Mediterranean littoral, about half-way between the region of distribution of the Sorghum bicolor subspecies verticilliflorum of tropical Africa and the southeast Asian populations of S. propinquum (Fig. 3). According to Doggett and Prasada Rao (11), S. halepense probably arose from chromosome doubling after a natural cross between these two species. S. halepense has also been introduced as a weed to all the warmer temperate regions of the world (8). Many ecotypes of S. halepense have been

4 reported (29). Though not widely acknowledged, two morphologically distinct complexes were reported within S. halepense: a Mediterranean tetraploid (2n=40 chromosomes) ecotype and a tropical diploid with 2n=20 chromosomes (9). To our knowledge, no further research has been carried out to confirm this. Within the Sorghum bicolor species, subspecies drummondii is the primary group of weedy sorghums that are strictly African. Sorghum shattercanes often appear in sympatry with the crop as hybrids resulting from crosses between cultivated and wild sorghums. Morphologically stabilized derivatives of shattercane often infest fields of grain sorghum and occur widely in farmers’ fields in India and the highlands of Ethiopia (8).

3. WEEDY SORGHUMS IN AGRO-ECO SYSTEMS

In general, weeds are harmful in most agro-ecosystems (43). S. halepense is reported as among the world’s 10 worst weed pests (23). S. halepense is an aggressive perennial grass described as a serious weed from the Mediterranean through the Middle East to India, Australia and the nearby islands, central and the Gulf coast of the United States. It has been reported as troublesome weed of numerous other important crops. S. halepense was introduced into the United States early in the nineteenth century as a crop before eventually becoming a pest, known in the Americas as johnsongrass (30). S. halepense is now classified as a noxious weed in 22 states in the USA and one province in Canada (http://invader.dbs.umt.edu). It is wind-pollinated, often found sympatric with grain sorghum virtually everywhere the crop is cultivated, and its flowering time often overlaps that of grain sorghum making genetic exchange very likely (23). Sorghum almum (Parodi), also called Columbus grass, does not present as much of a threat to agricultural systems as S. halepense, although it is wide spread (10). This perennial weed is classified as noxious in seven USA states. Weedy S. bicolor (shattercane) is an aggressive annual weed, which is well equipped with survival traits that allow it to readily out compete its cultivated progenitor. The shattering ability of the panicles of this weedy intermediate facilitates dispersal of and increases the likelihood for its survival in crop fields. Unlike S. halepense however, shattercanes lack rhizomes and are annual weeds. In highly mechanized , annual weeds are generally not hand pulled and thus their spread through dispersal is not controlled when they are able to over winter. Weedy sorghums are also detrimental to agriculture not only in terms of direct cost due to crop losses and chemical treatments, but also because they can serve as alternate hosts for pests and viruses that harm crops. For instance sorghum caused by Claviceps africana greatly reduces quality of grain in infected fields. Ergot can be a serious disease of seed parents in hybrid sorghum seed production fields, and the presence of ergot can, therefore, impact international seed markets. C. africana, a very specialized fungus that parasitizes only the flowers of specific grasses, survives in the conidial stage on feral sorghums and alternate hosts such as S. halepense (1). Furthermore, once established, C. africana could become endemic on S. halepense thus enhancing the risk. S. halepense is also a host for Colletotrichum graminicola, the anthracnose fungus. Isolates collected from S. halepense are highly pathogenic to sorghum (33).

4. GENE FLOW AMONG SORGHUMS

Natural outcrossing rate is variable among Sorghum bicolor strains and varieties. While preferentially self pollinated, outcrossing rates among sorghums can reach 26% for a grain-type

5 sorghum with compact panicle typical of commercial hybrids and 61% for an open grass-like panicle such as sudangrass (S. sudanensis) (36). Gene flow naturally exists between individuals that belong to different sorghum species and within or between gene pools. The most widely recognized interspecies sorghum weed, shattercane arises from the hybridization of subspecies bicolor and all wild relatives (20). Though not widely adopted, some also describe shattercanes as hybrids between sorghum crop and S. halepense (32). Outcrossing can also involve individuals with different ploidy levels. Sorghum almum is a tetraploid grass that arose from a natural cross between the tetraploid S. halepense and the diploid S. bicolor (10). The same weed is also described as an allopolyploid perennial weed resulting from the cross between S. propinquum and S. bicolor (14). Hybrids between grain sorghum (2n=20) and S. halepense (2n=40) can include highly sterile 30-chromosome and relatively fertile 40-chromosome types (19).

4.1 WEED TO CROP GENE FLOW

The flow of genes from wild and weedy types to landraces and improved crop cultivars is hard to detect in agricultural systems. However, landrace sorghum varieties maintain superiority over most improved sorghum cultivars in their arsenal of survival traits that may have been introgressed in them through time from their wild and weedy kin. Adaptation to harsh environment and competitiveness in agro-ecosystems are often important features of weeds, and it appears to be true for weedy sorghums as well. The prevalence of such traits in wild and weedy types has drawn some attention, in modern plant breeding, to their genetic potential as sources of agronomically useful genes for the improvement of the sorghum crop. Several studies were undertaken in recent years to search for genes of interest among wild and weedy types of sorghum. A high level of allelopathic activity was found in root exudates of S. halepense (7). Among traits of agronomic importance in sorghum, resistance to a highly virulent biotype E of the greenbug () was found in S. halepense (12). Resistance to ergot was found in the weedy type S. b. drummondii (37). The broad adaptation and perennial growth habit of S. halepense was reported as a source of valuable genes for improving sorghum (39). We have recently reported a unique source of resistance in S. b. drummondii to the parasitic weed , which plagues African sorghum (38). Wild sorghums are also a significant source of genes for crop improvement providing resistance sources to various biotic and abiotic stresses in the cultivated sorghum germplasm. The collection of wild sorghum germ plasm maintained at ICRISAT (461 accessions) has been evaluated for resistance to various pathogens and pests (25, 26). Wild sorghums with resistance to downy mildew, stem borer, shoot fly and midge were isolated. Furthermore, most of the greenbug (Biotype C) resistant sorghum hybrids currently grown in the US were originally derived from a wild sorghum source that belonged to race virgatum (12). Resistance to ergot was also found in several accessions of wild sorghum belonging to the arundinaceum subsp. (37). Because few, if any, organized studies have been undertaken on assessing weed to crop gene flow in sorghum, there is insufficient information on the rate and the extent of genetic exchange in situ. It is probable, based on the ease of cross pollination and the overlap in natural habitats, that there is a continual transfer of an array of fitness genes from weedy types to cultivated sorghum.

4.2 CROP TO WEED GENE FLOW

6

Natural gene flow between cultivated and wild and weedy sorghums in areas where they are sympatric has also led to gene exchange between the cultivated crop and wild relatives. Several studies (3, 39) showed that under natural conditions, crop-to-weed gene exchange is very likely in sorghum. Success in moving genes between crop and wild relatives depends on several factors including crossability, spontaneous hybridization, fertility, and fitness of the resultant hybrids. Potential hybridization of cultivated sorghum (S. bicolor) with sudangrass (S. sudanense) and its feral relatives (S. almum and S. halepense) was assessed for three congeners commonly growing in natural habitats near sorghum fields (2). However, although the potential for gene flow among this group of plants was recognized to be high, no deliberate study has been carried out, except for S. halepense, to characterize the extent of crossing and nature of hybrid progenies among these weedy species. Sangduen and Hanna (39) conducted chromosome and fertility studies on reciprocal crosses between tetraploid S. bicolor (autotetraploid induced by chemical treatment) and S. halepense. A relatively higher (71 to 83%) outcrossing rate was reported when S. halepense was the female parent compared to only 0 to 33% hybrids produced when the tetraploid S. bicolor was used as the seed parent. The study also showed that when S. halepense was used as the female parent, the average seed set on both selfed and open pollinated panicles were similar and high (from 82 to 95%). In contrast, when S. bicolor was used as the female parent, the average seed set was only 18% on selfed panicles, and as high as 74% on open pollinated panicles. Arriola and Ellstrand (3) devised an experiment to measure the incidence and rate of hybrid formation in the field. Their study revealed that hybrid seeds could be detected on panicles of S. halepense plants at distances up to 100 meters from the crop. Regardless of apparent variability among fields, years and distance, hybrid formation occurred at a range of 0-12% overall. Arriola and Ellstrand (4) conducted a fitness study of crop-weed hybrids of sorghum grown under field conditions to estimate the likelihood of persistence of hybrids in the wild. From their experiments, crop-weed hybrids were determined to be as fit as either of their parent plant for sexual characters as well as vegetative traits. However the authors tempered their results in suggesting an evaluation of hybrid fitness in wild conditions, without added irrigation. Fitness of hybrids obtained from crosses between grain sorghum (S. bicolor) and S. halepense was evaluated for potential propagation of the weed-gene in subsequent generations (19). The results showed that the highly sterile 30-chromosome hybrids have extremely vigorous rhizomes, and present a threat through vegetative reproduction. Conversely, the 40-chromosome hybrids, whether self-fertile or male- sterile, were found to be weakly rhizomatous and did not constitute a threat other than being a source of grassy weed seedlings.

4.3 CONSEQUENCES OF RECURRENT GENE FLOW

4.3.1 In conventional agriculture As briefly described earlier, distant relatives of sorghum, both wild and weedy-types, can be valuable sources of important genes for crop improvement. Wild and weedy species can also serve as a threat to modern agriculture. Agro-ecosystems can be severely affected by non monitored gene flow in which genes from landraces and elite germplasm are moved into the wild relative of the crop. The prevalence of such a gene exchange in sorghum and its potential effect on increasing the evolution of feral forms has only been studied in association with johnsongrass. However, intermediate forms such as the shattercanes readily appear in the agro-ecosystems in

7 much of Africa where sorghum cultivation is practiced without sufficient isolation from wild forms and in sympatry with weedy relatives. Progenies from an interspecific cross between sorghum and S. propinquum were genotyped with molecular markers and several quantitative trait loci associated to weediness were discovered (34). In the Americas, S. halepense has introgressed with grain sorghum to produce the widely distributed noxious weed. Derivatives of such introgression were described in Argentina as S. almum, a rhizomatous tetraploid grass that appears as a weed of sorghum. Enhanced weediness due to genetic exchange between wild and cultivated types is also illustrated by the ubiquitous and well-defined stable intermediates, the shattercanes, particularly in Africa (20). Several cases, among which S. almum was also listed, have been reported where invasive taxa have evolved after intertaxon hybridization (14). In some cases, such as in S. almum, invasiveness could possibly be a result of the fitness benefits conferred by heterosis. In evaluating the potential risk of genetic introgression into weedy types, therefore, fitness data is critical and need be determined. The other consequence of recurrent gene flow from crops to wild relatives is demographic swamping, which can occur following two different paths. A case of so-called “outbreeding depression” from detrimental gene flow can lead to reduced fitness of a locally rare species and eventually to its extinction (13). It is expected that domestication genes transferred into a weed might cause reduction in fitness as they might decrease the potential for weediness and lead to maladaptation (41). The other cause leading to demographic swamping is when a locally rare species loses its genetic integrity and becomes assimilated into a locally common species as a result of repeated bouts of hybridization (13, 27). Domesticated species have been implicated in the extinction or increased risk of extinction of wild species for two of the world’s 13 most important crops (13). The risk of extinction by hybridization depends on patterns of mating, and it is expected that the time to extinction by outbreeding depression and/or swamping will double if assortative mating is imposed over random mating more frequently. In sorghum, there may have been cases of genetic erosion, but only as a result of habitat change, despite cultivated sorghum growing adjacent to wild species, suggesting that genetic swamping is unlikely. We believe that consequences of recurrent gene flow between cultivated sorghum and its wild relatives need not be generalized, but considered on a case by case basis and in individual countries where the crop is grown. Sorghum offers an excellent example of the sympatric association and interaction of a crop-wild-weed complex of a species in an agro-ecosystem. The nature of genetic interaction among forms of the taxa and the consequences of these exchanges depend not only on the power of the genes involved but also on several other associated factors. Prevalence of wild relatives naturally varies from region to region based on extent of inherent genetic diversity, existence of selective pressures, and the farming systems in the region. Based primarily on knowledge of the agro-ecosystems and the history of genetic resource management and conservation, we have selected Ethiopia, Sudan, and the United States to demonstrate how different consequences may arise from gene flow between wild and cultivated sorghums. Although the empirical evidence we describe here is circumstantial and not experimental, it offers some basis for recognizing the differential effects of gene flow in contrasting ecological, demographical, and farming practices. Sudan and Ethiopia are the birth places of the crop and have witnessed the evolution of wild and primitive forms of sorghum. The USA is the largest producer of sorghum and likely to be one of the first places transgenic sorghums may be grown in commercial agriculture. Even though wild sorghums are not widely present in the Americas, the introduced weed S. halepense has been

8 reported in more than half the states of USA and having been described as a severe noxious weed in several states. 4.3.2 Introgression disrupted by genetic erosion Ethiopian sorghums are cultivated over a very large range of environments from 400 to 2,400 meters above sea level. Landraces have been selected for their specific adaptation and use for each of 18 major agro-ecological zones that characterize the country. Obviously, genetic exchange and interactions between wild and cultivated sorghum have taken place in Ethiopia. The recurrent gene flow that has existed for thousands of years, most probably acted upon by natural and deliberate selection, accounts for the present make-up of highly adapted and diverse forms of sorghum landraces in Ethiopia. Growing population pressure in recent years, recurrent drought, political strife, and persistent famine have forced farmers to practice extensive agriculture and to cultivate even the most marginal of land areas that formerly served as the natural habitat for wild and weedy species. Consequently, wild plant populations of sorghum have become a rarity in some regions of the sorghum growing areas of Ethiopia. As a result, few populations and patches of wild sorghums can be found. The prevalence of wild sorghums have been so severely reduced that the apparent potential gene flow between cultivated and wild sorghum has been significantly diminished. Genetic erosion in diversity of Ethiopian sorghums is apparent in both the wild and cultivated forms but is due to habitat loss, and not to genetic swamping. In patches where wild and weedy types are seen, hybrid forms are found that represent intermediate types with favorable traits from repeated events of hybridization that has taken place since the beginning of domestication of the crop. 4.3.3 In situ introgression in a natural habitat The scenario in the Sudan is different. Sudan has the largest land area in Africa, yet the population base in low, only a third of the population in Ethiopia. Per-capita holdings of arable land are higher in the Sudan than all other African countries. In northern Sudan, where human settlement has been historically very light, the genetic identity of wild sorghums may have been further protected by their isolation from human disturbance. In the central clay plains of the country where sorghum farming is practiced under irrigation and in rotation with other crops, wild sorghums have also survived as weed in cotton and fields and along the irrigation ditches (20). In both the rainfed and irrigated Sudanese agriculture, genetic exchange between sorghum and its wild relatives has resulted in formation of two widely recognized forms of crop- wild hybrids. Aggressive forms of weedy S. bicolor have evolved that are readily identified and recognized by most everyone as feral weeds, and known under a local name, “adar”. This is a form of shattercane that is widely distributed and almost accepted as unavoidable. In spite of continual weeding and selective roguing this weedy S. bicolor has not been easy to eradicate in Sudan. The second form of intermediate is equally feral, but appears more similar to cultivated sorghum and produces that only slowly shatter. Continued introgression of cultivated sorghum genes into wild forms has resulted in this hybrid form called “kerketita”. Farmers selectively harvest these types and encourage their continued existence, for they rely on them as feed and depending on the harvest prospect. In bad years, these fast growing intermediates provide the only harvest possible, particularly for fodder. We have recently started a study in Sudan to investigate the extent of gene introgression among these types and hope to assess the differential fitness of these introgressed intermediates in contrast to the cultivated and wild progenitors. 4.3.4 Introgression enhanced by modern farming practices

9 Sorghum and maize production in the USA has been severely affected by the widely recognized, highly competitive and noxious S. halepense. Mechanization favors perennial weed propagation as it stimulates rhizome growth. Because mechanized farming is practiced, farm implements used in plowing and cultivation in the US crop fields resulted in fortified rhizomes that spread readily and enhance the aggressiveness of the perennial weed. Aggressiveness of weeds can further be enhanced by the introgression of genes from highly improved cultivars as long as these genes confer an advantage. Continuous crossing, however low the frequency, also generates hybrid progeny that are ever more vigorous. These resultant hybrids possess additional fitness benefits conferred on to them via heterosis. A successful transfer of fitness from cultivated sorghum into weedy types is best illustrated in the creation of a now famous crop, sudangrass (Sorghum sudanense). This forage grass resulted from the introgression of cultivated sorghum genes into the weedy germplasm of Sorghum sudanense. It probably evolved during the millennia of genetic exchange among sorghum species in the Sudan. It combines excellent attributes of cultivated and wild sorghums that allow effective regeneration of seeds as well as fast crop development and re-growth after repeated cuts as a fodder. Sorghum-sudan are the most widely commercialized forage crop in the world, perhaps next to alfalfa.

4.4 IN THE TRANSGENIC ERA

The expectation of reduced fitness brought about by domestication genes transferred to wild recipient genome may not hold for transgenic traits that confer herbicide resistance, or other fitness enhancing traits. In most case transgenes added to highly domesticated crops are not anticipated to survive in nature without human intervention, as shown for , oilseed rape, maize and sugar beet (6). However, partially domesticated crops may constitute an exception for the dependency on humans. Assessment of the survival of transgenes in nature requires considering the impact of the performance of transgenic plants under field conditions, i.e., tolerance to abiotic stresses or pest resistance, as well as the feral tendency of crops. When transgenic traits are not expected to increase plant fitness in natural habitats, such as herbicide resistance, the risk of its persistence in the wild is lessened. However, when transgenes are transferred into forage crops to confer herbicide resistance, increased weediness may occur by reducing the opportunities to control feral populations (16). Many domestication genes are presumed to represent a loss rather than a gain of function, as indicated by their recessiveness. Exception is found in sorghum where action of S. propinquum allele for reduced seed size were mainly (67% of the alleles) recessive to the corresponding S. bicolor alleles (35). For a species with a relatively high outcrossing rate such as sorghum, dominant mutations may have been easily selected during the domestication process, mostly for a trait such as seed size which is under strong selective pressure. In contrast to domestication genes favored in agro-ecosystems transgenes frequently represent gains of function that might release wild relatives from constraints that limit their fitness, but often make crops less adapted to natural ecosystems, (17). Whether gene flow from a transgenic crop to its wild relative can lead to transgene escape and long-term survival, imply asking whether the transgene will effectively introgress and add to fitness of the wild population. The question is broader than the elements we addressed in this review. Undoubtedly gene flow exists between cropped sorghum and its wild relatives, and transfer of transgenes from a genetically engineered sorghum is likely. The prevalence of wild

10 relatives in the vicinity of the transgenic crop, as would be true in centers of , significantly increases this likelihood. For a gene to introgress into a wild relative it is necessary that repeated backcrosses and stabilization of the transgene occur in the new host. The likelihood of transgene introgression into a wild relative will depend on its dominance, absence of association with deleterious crop alleles or traits and the location in the genome. The speed in which the transgene introgresses and stabilizes in the population will depend on selective pressure and population size. Furthermore, the nature of the allele that is introgressed and whether or not the function gained as a result of the introgession contributes to fitness and ferality are key considerations. Important questions remain to be considered to assess the risk of transgene introgression into the wild gene pool. What is the actual magnitude of gene flow (both through pollen and seed) in different agro-ecostystems? Will the interactive effects of the introduced alleles and the management practices in the agro-ecosystems force selection of aggressive hybrids? How do transgenes behave (expression and stability) in wild genetic backgrounds? Will transgenes be preferentially selected in the wild populations, and will they persist? These and perhaps many other similar questions are currently under investigation in several laboratories, including our own. The lessons we learn should offer empirical evidence on the degree of gene flow within and among related taxa as well as what can be devised to mitigate serious consequences that may arise from the evolution of feral forms.

5. LITERATURE CITED

1. Alderman S, Frederickson D, Milbrath G, Montes N, Narro-Sanchez J, Obdvody G. 1999. A laboratory guide to the identification of Claviceps purpurea and Claviceps Africana in grass and sorghum seed samples. http://oda/state.or.edu 2. Arriola PE. 2002. Gene flow and hybrid fitness in the Sorghum bicolor - Sorghum halepense complex. Presented at Gene Flow Workshop, Ohio State University, March 5 and 6, 2002. http://www.biosci.ohio-state.edu/~asnowlab/Proceedings.pdf 3. Arriola PE, Ellstrand NC. 1996. Crop-to-weed gene flow in the genus Sorghum (Poaceae): spontaneous interspecific hybridization between johnsongrass, Sorghum halepense, and crop sorghum, S. bicolor. Am. J. Bot. 83: 1153-60 4. Arriola PE, Ellstrand NC. 1997. Fitness of interspecific hybrids in the genus Sorghum: persistence of crop genes in wild population. Ecol. Applic. 7: 512-8 5. Casas A, Kononowicz A, Zehr U, Tomes D, Axtell J, et al. 1993. Transgenic sorghum plants via microprojectile bombardment. Proc. Natl. Acad. Sci. USA 90: 11212-6 6. Crawley MJ, Brown SL, Hails RS, Kohn DD, Ress M. 2001. Transgenic crops in natural habitats. Nature 409: 682-3 7. Czarnota MA, Rimando AM, Weston LA. 2003. Evaluation of root exudates of seven sorghum accessions. J. Chem. Ecol. 29: 2073-83 8. de Wet JMJ. 1978. Systematics and evolution of sorghum sect. Sorghum (Gramineae). Amer. J. Bot. 65: 477-84 9. de Wet JMJ, Huckabay JP. 1967. The origin of Sorghum bicolor. II. Distribution and domestication. Evolution 21: 787-802 10. Doggett H. 1988. Sorghum. New York: Wiley & Sons. 403 pp. 11. Doggett H, Prasada Rao KE. 1995. Sorghum. In Evolution of crop plants, ed. J Smartt, NW Simmonds, pp. 173-80. London/New York: Longmans

11 12. Duncan RR, Bramel-Cox PJ, Miller FR. 1991. Contributions of introduced germplasm to hybrid development in the USA. In Use of plant introductions in cultivar development, ed. HL Shands, L Weisner, pp. 69-102. CSSA Special Publication no. 17 13. Ellstrand NC, Prentice HC, Hancock JF. 1999. Gene flow and introgression from domesticated plants into their wild relatives. Ann. Rev. Ecol. Syst. 30: 539-63 14. Ellstrand NC, Schierenbeck KA. 2000. Hybridization as a stimulus for the evolution of invasiveness in plants? Proc. Natl. Acad. Sci. USA 97: 7043-50 15. FAOSTAT. 2003. http://faostat.fao.org 16. Gepts P. 2002. A comparison between crop domestication, classical plant breeding, and genetic engineering. Crop Sci. 42: 1780-90 17. Gepts P, Papa R. 2003. Possible effects of (trans)gene flow from crops on the genetic diversity from landraces and wild relatives. Environ. Biosafety Res. 2: 89-103 18. Grenier C, Bramel PJ, Dahlberg JA, El-Ahmadi A, Mahmoud M, et al. 2004. Sorghums of the Sudan: analysis of regional diversity and distribution. Genet. Resour. Crop Evol. 51: 489-500 19. Hadley HH. 1958. Chromosome numbers, fertility and rhizome expression of hybrids between grain sorghum and johnsongrass. J. Agron. 50: 278-82 20. Harlan JR. 1992. Crops and man. Madison, WI: American Society of Agronomy. 284 pp. 21. Harlan JR, de Wet JMJ. 1971. Toward a relational classification of cultivated plants. Taxon 20: 509-17 22. Harlan JR, de Wet JMJ. 1972. A simplified classification of cultivated sorghum. Crop Sci. 12: 172-7 23. Holm LG, Plucknett DL, Pancho JV, Herberger JP. 1977. The world's worst weeds, distribution and biology. Honolulu: University Press of Hawaii. pp 54-61 24. Jeoung JM, Krishnaveni S, Muthukrishnan S, Trich HN, Liang GH. 2002. Optimization of sorghum transformation parameters using genes for green fluorescent protein and β- glucuronidase as visual markers. Hereditas 137: 20-8 25. Kamala V, Singh SD, Bramel PJ, Rao DM. 2002. Sources of resistance to downy mildew in wild and weedy sorghums. Crop Sci. 42: 1357-60 26. Kameswara Rao N, Reddy LJ, Bramel PJ. 2003. Potential of wild species for genetic enhancement of some semi-arid food crops. Genet. Resour. Crop Evol. 50: 707-21 27. Levin DA, Francisco-Ortega J, Jansen RK. 1996. Hybridization and the extinction of rare plant species. Conserv. Biol. 10: 10-6 28. Mann JA, Kimber CT, Miller FR. 1983. The origin and early cultivation of sorghums in Africa. Tex. Agric. Exp. Stn. Bull. 1454. 21 pp. 29. McWhorter CG. 1971. Growth and development of johnsongrass ecotypes. Weed Sci. 19: 141-6 30. McWhorter CG. 1971. Introduction and spread of johnsongrass in the United States. Weed Sci. 19: 496-500 31. Murty BR, Arunachalam V, Saxena MBL. 1967. Classification and catalogue of a world collection of sorghum. Indian J. Genet. Plant Breed. 27: 1-394 32. OTA. 1993. Harmful non-indigenous species in the United States. Washington, D.C.: Office of Technology Assessment, U.S. Government Printing Office 33. Pastor-Corrales MA, Frederiksen RA. 1978. Sorghum anthracnose. Presented at International Workshop on Sorghum diseases - A world review. Hyderabad, India: ICRISAT

12 34. Paterson A, Schertz K, Lin Y, Liu S, Chang Y. 1995. The weediness of wild plants: molecular analysis of genes influencing dispersal and persistence of johnsongrass, Sorghum halepense (L.) Pers. Proc. Natl. Acad. Sci. USA 92: 6127-31 35. Paterson A, Schertz K, Lin Y, Li Z. 1998. Case history in plant domestication: sorghum, an example of cereal evolution. In Molecular dissection of complex traits, ed. A Paterson, pp. 187-95 Boca Raton, Florida: CRC Press 36. Pedersen J, Toy J, Johnson B. 1998. Natural outcrossing of sorghum and sudangrass in the central great plains. Crop Sci. 38: 937-9 37. Reed JD, Ramundo BA, Claflin LE, Tuinstra MR. 2002. Analysis of resistance to ergot in sorghum and potential alternate hosts. Crop Sci. 42: 1135-8 38. Rich PJ, Grenier C, Ejeta G. 2004. Striga resistance in wild relative of sorghum. Crop Sci. 44: In press 39. Sangduen N, Hanna WW. 1984. Chromosome and fertility studies on reciprocal crosses between two species of autotetraploid sorghum. J. Hered. 75: 293-6 40. Snowden JD. 1936. The cultivated races of sorghum. London: Adlard & Son, Ltd. 41. Stewart CN, Halfhill MD, Warwick SI. 2003. Transgene introgression from genetically modified crops to their wild relatives. Nature Rev. Genet. 4: 806-17 42. Vavilov NI. 1951. The origin, variation, immunity and breeding of cultivated plants. Chron. Bot. : 1-366 43. Westbrooks RG. 1998. Invasive plants: changing the landscape of America: Fact book. Federal Interagency Committee for the Management of Noxious and Exotic Weeds, Washington, D.C. 109 pp. 44. Zhao Z-Y, Cai T, Tagliani L, Miller M, Wang N, et al. 2000. Agrobacterium-mediated sorghum transformation. Plant Mol. Biol. 44: 789-98

13 Figure 1. The sorghum taxa: the sorghum genus is a member of five major sub-genera in the Poaceae family. Species bicolor is the cogenitor of the crop-wild-weed complex in the sorghum genus.

14 Figure 2. The sorghum gene pool based on classification of a "biological species" as per Harlan and de Wet (21).

Figure 3. Pattern of domestication and spread of the genus Sorghum.

15